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Immunohistochemical localization of chondroitin sulfate proteoglycan and tenascin in the human eye compared with the HNK-1 epitope

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Abstract

•Background: A previous study revealed the HNK-1 epitope in the human ciliary body beneath the ciliary epithelium. The molecules bearing this 3-sulphoglucuronic acid-containing oligosaccharide epitope in the eye remain unknown. As chondroitin sulphate proteoglycan (CSPG) and tenascin are potential candidates as bearers of the HNK-1 epitope, their distribution in the human eye was compared with that of the HNK-1 epitope. • Methods: Fifty-five formalin-fixed, paraffin-embedded human eyes, including 20 normal eyes and 35 eyes with exfoliation syndrome or glaucoma, were studied immunohistochemically with monoclonal antibody (MAb) CS-56 to CSPG, MAb TN2 to tenascin, and MAbs HNK-I and VC1.1 to the HNK-1 epitope. Additionally, four frozen lens capsules with exfoliation material were studied by indirect immunofluoresence. • Results: A population of dendritic cells in the inner connective tissue layer of the ciliary body and exfoliation material were immunoreactive with antibodies to the HNK-1 epitope, but no labelling for CSPG and tenascin was seen in them, including frozen sections. The inner surface of the nonpigmented ciliary epithelium was reactive for the HNK-1 epitope, and at the ora serrata also for CSPG. In some eyes with glaucoma, immunoreaction for CSPG and tenascin was seen beneath the epithelium and endothelium of the cornea. The nerve fibre layer of the retina was labelled for tenascin. In the sclera, all antibodies labelled the ground substance, and in some large blood vessels immunoreaction for CSPG and tenascin was seen subendothelially. • Conclusion: Apart from the sclera, the distribution of CSPG and tenascin was different from that of the HNK-1 epitope, suggesting that this carbohydrate epitope may not be borne by these molecules in the human ciliary body.

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References

  1. Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol 127:1024–1029

    Google Scholar 

  2. Aoyama N, Kikawada R, Yamashina SY (1993) Immunohistochemical study on the development of the rat heart conduction system using anti-Leu-7 antibody. Arch Histol Cytol 56:303–315

    Google Scholar 

  3. Arimatsu Y, Naegele JR, Barnstable CJ (1987) Molecular markers of neuronal subpopulations in layers 4, 5, and 6 of cat primary visual cortex. J Neurosci 7:1250–1263

    Google Scholar 

  4. Avnur Z, Geiger B (1984) Immunocytochemical localization of native chondroitin sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38:811–822

    Google Scholar 

  5. Baba H (1983) Histochemical and polarization optical investigation for glycosaminoglycans in exfoliation syndrome. Graefe's Arch Clin Exp Ophthalmol 221:106–109

    Google Scholar 

  6. Bollensen E, Schachner M (1987) The peripheral myelin glycoprotein Po expresses the L2/HNK-1 and L3 carbohydrate structures shared by neural adhesion molecules. Neurosci Lett 82:77–82

    Google Scholar 

  7. Bon S, Méflah K, Musset F, Grassi J, Massoulié J (1987) An immunoglobulin M monoclonal antibody, recognizing a subset of acetylcholinesterase molecules from electric organs of Electrophorus and Torpedo, belongs to the HNK-1 anti-carbohydrate family. J Neurochem 49:1720–1731

    Google Scholar 

  8. Chou DKH, Ilyas AA, Evans JE, Costello C, Quarles RH, Jungalwala FB (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy. J Biol Chem 261:11717–11725

    Google Scholar 

  9. Daugaard S, Strange L, Schiødt T (1991) Immunohistochemical staining for chondroitin sulphate and keratan sulphate. An evaluation of two monoclonal antibodies. Histochemistry 95:585–589

    Google Scholar 

  10. Faissner A, Kruse J, Chiquet-Ehrismann R, Mackie E (1988) The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin. Differentiation 37:104–114

    Google Scholar 

  11. Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and nonneural tissues that mediates glia-neuron interaction. Proc Nail Acad Sci USA 82:8075–8079

    Google Scholar 

  12. Hageman GS, Johnson LV (1987) Chondroitin 6-sulfate glycosaminoglycan is a major constituent of primate cone photoreceptor matrix sheaths. Curr Eye Res 6:639–646

    Google Scholar 

  13. Hoffman S, Edelman GM (1987) A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc Natl Acad Sci USA 84:2523–2527

    Google Scholar 

  14. Hogan MJ, Alvarado JA, Weddel JE (1971) Histology of the human eye. An atlas and textbook. Saunders, Philadelphia, pp 260–319

    Google Scholar 

  15. Kitada S, Shapourifar-Tehrani S, Smyth RJ, Lee DA (1991) Characterization of human and rabbit pigmented and nonpigmented ciliary body epithelium. Curr Eye Res 10:409–415

    Google Scholar 

  16. Kivelä T (1986) Expression of the HNK-1 carbohydrate epitope in human retina and retinoblastoma. An immunohistochemical study with the anti-Leu-7 monoclonal antibody. Virchows Arch [A] 410:139–146

    Google Scholar 

  17. Koukoulis GK, Gould VE, Bhattacharyya A, Gould JE, Howeedy AA, Virtanen I (1991) Tenascin in normal, reactive, hyperplastic, and neoplastic tissues: biologic and pathologic implications. Hum Pathol 22:636–643

    Google Scholar 

  18. Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis C, Schachner M (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 311:153–155

    Google Scholar 

  19. Kruse J, Keilhauer G, Faissner A, Timpl R, Schachner, M. (1985) The J1 glycoprotein — a novel nervous system cell adhesion molecule of the L2/ HNK-1 family. Nature 316:146–148

    Google Scholar 

  20. Lallier T, Bronner-Fraser M (1992) α1ß1 Integrin on neural crest cells recognizes some laminin substrata in a Ca2+-independent manner. J Cell Biol 119:1335–1345

    Google Scholar 

  21. Lightner VA, Gumkowski F, Bigner DD, Erickson HP (1989) Tenascin/Hexabrahion in human skin: biochemical identification and localization by light and electron microscopy. J Cell Biol 108:2483–2493

    Google Scholar 

  22. Margolis RK, Ripellino JA, Goossen B, Steinbrich R, Margolis RU (1987) Occurrence of the HNK-1 epitope (3-sulfoglucuronic acid) in PC12 pheochromocytoma cells, chromaffin granule membranes, and chondroitin sulfate proteoglycans. Biochem Biophys Res Commun 145:1142–1148

    Google Scholar 

  23. Marshall GE, Konstas AGP, Abraham S, Lee WR (1992) Extracellular matrix in aged human ciliary body: an immunoelectron microscope study. Invest Ophthalmol Vis Sci 33:2546–2560

    Google Scholar 

  24. McGarry RC, Helfand SL, Quarles RH, Roder JC (1983) Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 306:376–378

    Google Scholar 

  25. Nordlander RH (1993) Cellular and subcellular distribution of HNK-1 immunoreactivity in the neural tube of Xenopus. J Comp Neurol 335:538–551

    Google Scholar 

  26. Perentes E, Herbort CP, Rubinstein LJ, Herman MM, Uffer S, Donoso LA, Collins VP (1987) Immunohistochemical characterization of human retinoblastomas in situ with multiple markers. Am J Ophthalmol 103:647–658

    Google Scholar 

  27. Perez RG, Halfter W (1993) Tenascin in the developing chick visual system: distribution and potential role as a modulator of retinal axon growth. Dev Biol 156:278–292

    Google Scholar 

  28. Pesheva P, Horwitz AF, Schachner M (1987) Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules. Neurosci Lett 83:303–306

    Google Scholar 

  29. Rittig M, Lütjen-Drecoll E, Rauterberg J, Jander R, Mollenhauer J (1990) Type-VI collagen in the human iris and ciliary body. Cell Tissue Res 259:305–312

    Google Scholar 

  30. Schlötzer-Schrehardt U, Dörfler S, Naumann GOH (1992) Immunohistochemical localization of basement membrane components in pseudoexfoliation material of the lens capsule. Curr Eye Res 11:343–355

    Google Scholar 

  31. Schlötzer-Schrehardt U, Küchle M, Dörfler S, Naumann GOH (1993) Pseudoexfoliative material in the eyelid skin of pseudoexfoliation-suspect patients: a clinico-histopathological correlation. Ger J Ophthalmol 2:51–60

    Google Scholar 

  32. Tawara A, Varner HH, Hollyfield JG (1989) Distribution and characterization of sulfated proteoglycans in the human trabecular tissue. Invest Ophthalmol Vis Sci 30:2215–2231

    Google Scholar 

  33. Tervo K, Tervo T, van Setten GB, Tarkkanen A, Virtanen I (1989) Demonstration of tenascin-like immunoreactivity in rabbit corneal wounds. Acta Ophthalmol 67:347–350

    Google Scholar 

  34. Tervo T, van Setten GB, Lehto I, Tervo K, Tarkkanen A, Virtanen I (1990) Immunohistochemical demonstration of tenascin in the normal human limbus with special reference to tra beculectomy. Ophthalmic Res 22:128–133

    Google Scholar 

  35. Uusitalo M, Kivela T, Tarkkanen A (1993) Identification of a novel element in the human eye: the inner connective tissue layer of the ciliary body characterized with antibodies to the HNK-1 epitope. Invest Ophthalmol Vis Sci 34:2372–2381

    Google Scholar 

  36. Uusitalo M, Kivelä T, Tarkkanen A (1993) Immunoreactivity of exfoliation material for the cell adhesion-related HNK-1 carbohydrate epitope. Arch Ophthalmol 111:1419–1423

    Google Scholar 

  37. Uusitalo M, Kivela T, Tarkkanen A (1994) The HNK-1 epitope in the inner connective tissue layer of the human ciliary body in exfoliation syndrome and various types of glaucoma. Graefe's Arch Clin Exp Ophthalmol 232:8–15

    Google Scholar 

  38. Zaremba S, Naegele JR, Barnstable CJ, Hockfield S (1990) Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VCL1. J Neurosci 10:2985–2995

    Google Scholar 

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Uusitalo, M. Immunohistochemical localization of chondroitin sulfate proteoglycan and tenascin in the human eye compared with the HNK-1 epitope. Graefe's Arch Clin Exp Ophthalmol 232, 657–665 (1994). https://doi.org/10.1007/BF00171380

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  • DOI: https://doi.org/10.1007/BF00171380

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